Inbreeding depression and haplodiploidy: experimental measures in a parasitoid and comparisons across diploid and haplodiploid insect taxa

Abstract. It has long been assumed that inbreeding depression in haplodiploid organisms is low due to their ability to purge genetic load in haploid males. It has been suggested that this low genetic load could facilitate the evolution of inbreeding behaviors driven by local mate competition in hymenopteran parasitoids. I have examined inbreeding depression in haplodiploids in two ways. First I show that an outbreeding haplodiploid wasp Uscana semifumipennis (Hymenoptera: Trichogrammatidae) suffers substantial inbreeding depression. Longevity was 38% shorter, fecundity was 32% lower, and sex ratio was 5% more male for experimentally inbred wasps when compared to outbred controls. There were interactions between size and both fecundity and sex ratio for inbred wasps that were not seen for outbred individuals. Second, an analysis of data from the literature suggests that when inbreeding is experimentally imposed on populations, haplodiploid insects and mites as a group do suffer less from inbreeding depression than diploid insects, although substantial inbreeding depression in haplodiploid taxa does exist. The meta-analysis revealed no difference in inbreeding depression between gregarious haplodiploid wasps, which are likely to have a history of inbreeding, and solitary haplodiploid species, which are assumed to be primarily outbred.     

Between- and within-host species selection on cytoplasmic incompatibility-inducing Wolbachia in haplodiploids

Abstract The most common effect of the endosymbiont Wolbachia is cytoplasmic incompatibility (CI), a form of postzygotic reproductive isolation that occurs in crosses where the male is infected by at least one Wolbachia strain that the female lacks. We revisited two puzzling features of Wolbachia biology: how Wolbachia can invade a new species and spread among populations, and how the association, once established in a host species, can evolve, with emphasis on the possible process of infection loss. These questions are particularly relevant in haplodiploid species, where males develop from unfertilized eggs, and females from fertilized eggs. When CI occurs in such species, fertilized eggs either die (female mortality type: FM), or develop into males (male development type: MD), raising one more question: how transition among CI types is possible. We reached the following conclusions: (1) the FM type is a better invader and should be retained preferentially after a new host is captured; (2) given the assumptions of the models, FM and MD types are selected on neither the bacterial side nor the host side; (3) selective pressures acting on both partners are more or less congruent in the FM type, but divergent in the MD type; (4) host and symbiont evolution can drive infection to extinction for all CI types, but the MD type is more susceptible to the phenomenon; and (5) under realistic conditions, transition from MD to FM type is possible. Finally, all these results suggest that the FM type should be more frequent than the MD type, which is consistent with the results obtained so far in haplodiploids.     

CYTONUCLEAR THEORY FOR HAPLODIPLOID SPECIES AND X-LINKED GENES. II. STEPPING-STONE MODELS OF GENE FLOW AND APPLICATION TO A FIRE ANT HYBRID ZONE

We develop cytonuclear, hybrid zone models for haplodiploid species or X-linked genes in diploid species using a stepping-stone framework of migration, in which migration rates vary with both direction and sex. The equilibrium clines for the allele frequencies, cytonuclear disequilibria, and frequencies of pure parental types are examined for species with diagnostic markers, under four important migration schemes: uniform migration of both sexes in both directions, greater migration of both sexes from one direction, greater migration of females, and greater migration of males. Of the three cytonuclear variables examined, the allele frequency clines are the most informative in differentiating among the various migration patterns. The cytonuclear disequilibria and the frequency of the pure parental types tend to be useful only in revealing directional asymmetries in migration. The extent of hybrid zone subdivision has quantitative but not qualitative effects on the distribution of cytonuclear variables, in that the allele frequency clines become more gradual, the cytonuclear disequilibria decrease in magnitude, and the frequencies of pure parentals decline with increasing subpopulation number. Also, the only major difference between the X-linked and haplodiploid frameworks is that a higher frequency of pure parentals is found when considering haplodiploids, in which male production does not require mating. The final important theoretical result is that censusing after migration yields greater disequilibria and parental frequencies than censusing after mating. We analyzed cytonuclear data from two transects from a naturally occurring hybrid zone between two haplodiploid fire ant species, Solenopsis invicta and S. richteri, using our stepping-stone framework. The frequency of S. invicta mtDNA exceeds the frequency of the S. invicta nuclear markers through much of this hybrid zone, indicating that sex differences in migration or selection may be occurring. Maximum-likelihood estimates for the migration rates are very high, due to an unexpectedly large number of pure parental types in the hybrid zone, and differ substantially between the two transects. Overall, our model does not provide a good fit, in part because the S. invicta–S. richteri hybrid zone has not yet reached equilibrium.     

Sex allocation in haplodiploids is mediated by egg size: evidence in the spider mite Tetranychus urticae Koch

Haplodiploid species display extraordinary sex ratios. However, a differential investment in male and female offspring might also be achieved by a differential provisioning of eggs, as observed in birds and lizards. We investigated this hypothesis in the haplodiploid spider mite Tetranychus urticae, which displays highly female-biased sex ratios. We show that egg size significantly determines not only larval size, juvenile survival and adult size, but also fertilization probability, as in marine invertebrates with external fertilization, so that female (fertilized) eggs are significantly larger than male (unfertilized) eggs. Moreover, females with on average larger eggs before fertilization produce a more female-biased sex ratio afterwards. Egg size thus mediates sex-specific egg provisioning, sex and offspring sex ratio. Finally, sex-specific egg provisioning has another major consequence: male eggs produced by mated mothers are smaller than male eggs produced by virgins, and this size difference persists in adults. Virgin females might thus have a (male) fitness advantage over mated females.     

Sex biased intra-tree oviposition site selection and larval foraging behavior of a specialist herbivore

Heterogeneity in the quality of oviposition and feeding sites within plants can significantly influence the distribution and abundance of herbivorous insects, but remains poorly understood. Field surveys and a manipulative study were conducted to evaluate the influence of variation within the crown of black spruce, Picea mariana (Mill.) B.S.P. (Pinaceae), on adult oviposition and larval feeding behavior of yellowheaded spruce sawfly, Pikonema alaskensis Rohwer (Hymenoptera: Tenthredinidae). Most eggs were laid in the mid to lower crown of 1.5–2 m tall trees. However, most of the few eggs that were laid in the upper crown (i.e., whorl 2) were female. Fourth and fifth instars dispersed acropetally, from the mid and lower to the upper crown, causing high defoliation in the upper crown. Late-instar females were generally more abundant than males on the leader, the most apical shoot on a tree where eggs and early instars rarely occurred, strongly suggesting that more females than males disperse acropetally. This hypothesis was supported in a manipulative experiment, where only 15–20% of larvae in all-male broods, but almost three-quarters of larvae in mixed broods, dispersed to the upper crown. To our knowledge, this is only the second study to explicitly demonstrate preferential allocation of progeny sex through oviposition site selection by a herbivorous insect, and the first study to unambiguously demonstrate sex-biased dispersal by the juveniles of an insect whose adult females can fly. This study emphasizes the important role of intra-plant variation in shaping both oviposition site selection and the dispersal behavior of juvenile phytophagous insects within their hosts, and suggests that sex-biased foraging behaviors may be necessary for some insects to accommodate the respective needs of immature females and males within heterogeneous host plants.     

Epigenetic inheritance and genome regulation: is DNA methylation linked to ploidy in haplodiploid insects?

Organisms show great variation in ploidy level. For example, chromosome copy number varies among cells, individuals and species. One particularly widespread example of ploidy variation is found in haplodiploid taxa, wherein males are typically haploid and females are typically diploid. Despite the prevalence of haplodiploidy, the regulatory consequences of having separate haploid and diploid genomes are poorly understood. In particular, it remains unknown whether epigenetic mechanisms contribute to regulatory compensation for genome dosage. To gain greater insights into the importance of epigenetic information to ploidy compensation, we examined DNA methylation differences among diploid queen, diploid worker, haploid male and diploid male Solenopsis invicta fire ants. Surprisingly, we found that morphologically dissimilar diploid males, queens and workers were more similar to one another in terms of DNA methylation than were morphologically similar haploid and diploid males. Moreover, methylation level was positively associated with gene expression for genes that were differentially methylated in haploid and diploid castes. These data demonstrate that intragenic DNA methylation levels differ among individuals of distinct ploidy and are positively associated with levels of gene expression. Thus, these results suggest that epigenetic information may be linked to ploidy compensation in haplodiploid insects. Overall, this study suggests that epigenetic mechanisms may be important to maintaining appropriate patterns of gene regulation in biological systems that differ in genome copy number.     

Manipulation of oviposition choice of the parasitoid wasp, Encarsia pergandiella, by the endosymbiotic bacterium Cardinium

Reproductive manipulations of hosts by maternally inherited bacterial endosymbionts often result in an increase in the proportion of infected female hosts in the population. When this involves the conversion of incipient males to genetic or functional females, it presents unique difficulties for symbionts invading hosts with sex-specific reproductive behaviours, such as the autoparasitic Encarsia pergandiella. In sexual forms of this species, female eggs are laid in whitefly nymphs and male eggs are laid in conspecific or heterospecific parasitoids developing within the whitefly cuticle. Further, eggs laid in the 'wrong' host do not ordinarily complete development. This study explored the role of a bacterial symbiont, Cardinium, in manipulating oviposition behaviour in a thelytokous population of E. pergandiella. Oviposition choice was measured by the number and location of eggs deposited by both infected and uninfected adult waSPS in arenas containing equal numbers of hosts suitable for the development of male and female waSPS. Uninfected waSPS included antibiotic-treated female waSPS and (untreated) daughters of antibiotic-treated female waSPS. The choices of waSPS in the thelytokous population treatments were compared with those of a conspecific sexual population. We found that offspring of antibiotic-cured thelytokous waSPS reverted to the behaviour of unmated sexual waSPS, laying their few eggs almost exclusively in hosts appropriate for male eggs. Infected thelytokous waSPS distributed their eggs approximately evenly between host types, much like mated sexual female waSPS. The antibiotic-treated female waSPS exhibited choices intermediate to waSPS in the other two treatments. The change in the observed behaviour appears sufficient to allow invasion and persistence of Cardinium in sexual populations. Lastly, our results suggest a reduction in host discrimination as a possible mechanism by which Cardinium influences this change.     

Evidence for an even sex allocation in haplodiploid cyclical parthenogens

Recent theoretical work has shown that haplodiploid cyclical parthenogens, such as rotifers, are expected to have an equal frequency of male‐producing and resting‐egg producing females during their sexual phase. We tested this prediction by following sexual reproduction dynamics in two laboratory populations and one field population of the rotifer Brachionus plicatilis through two growing seasons. We recorded population density, proportion of sexual females, and sex allocation (the proportion of male‐producing sexual females as a fraction of total sexual females). We found this sex allocation ratio to vary from 0.3 to 1.0 in single sampling events. However, when we computed sex allocation by using the integrated densities of both male‐producing sexual females and resting‐egg producing sexual females over time, the two laboratory populations and one of the two field growing seasons showed sex allocation ratios that did not significantly differ from the expected value of 0.5.